morphological diversity of microstructures occurring in selected recent bivalve shells and their ecological implications

Contemp.Trends.Geosci., 5(2),2016,104-112 DOI:10.1515/ctg-2016-0008 Morphological diversity of microstructures occurring in selected recent bivalve shells and their ecological implications Krzysztof Roman Brom*, Krzysztof Szopa Faculty of Earth Sciences, University of Silesia, ul Będzińska 60, 41-200 Sosnowiec, Poland *Correspondence: kbrom@us.edu.pl Received: 17th August, 2016 Accepted: 17th November, 2016 Abstract Environmental adaptation of molluscs during evolution has led to form biomineral exoskeleton – shell The main compound of their shells is calcium carbonate, which is represented by calcite and/or aragonite The mineral part, together with the biopolymer matrix, forms many types of microstructures, which are differ in texture Different types of internal shell microstructures are characteristic for some bivalve groups Studied bivalve species (freshwater species – duck mussel (Anodonta anatina Linnaeus, 1758) and marine species – common cockle (Cerastoderma edule Linnaeus, 1758), lyrate Asiatic hard clam (Meretrix lyrata Sowerby II, 1851) and blue mussel (Mytilus edulis Linnaeus, 1758)) from different locations and environmental conditions, show that the internal shell microstructure with the shell morphology and thickness have critical impact to the ability to survive in changing environment and also to the probability of surviving predator attack Moreover, more detailed studies on molluscan structures might be responsible for create mechanically resistant nanomaterials Key words: shell, calcium carbonate, microstructures, biomineral, anti-predator adaptations necessity of mechanical protection of soft tissues with impaired ability to regenerate (Pokryszko 2009; Jackson et al 2010; Vendrasco et al 2010) Further, pressure from shell-crushing and shell-drilling predators results in origin of appropriate shell microstructures, in order to increase mechanical strength of shell (Taylor and Layman 1972; Ragaini and Di Celma 2009; Kosnik et al 2011) Bivalve shell is the product of mantle (pallium) and it is composed mainly of calcium carbonate (in the form of calcite and/or aragonite), which constitutes at least 95 % of its weight, and the biopolymers forming organic matrix (Dyduch-Falniowska and Piechocki 1993; Barthelat et al 2009; Piechocki 2009; Katti et al 2010; Meyers et al Introduction Biomineral exoskeletons frequently exhibit unique hierarchical internal structures, which increase mechanical strength of them Organisms which evolve in the environment, where they are constantly exposed to unfavourable environmental factors, generally use them as a protecting armor or to strengthen their bodies Examples of such organisms are shelly faunas (like Mollusca), which possess shells made mainly of calcium carbonate (Vincent et al 2006; Futuyma 2008; Barthelat et al 2009; Brom et al 2015) Early molluscs species, probably in order to reduce pressure from predators, adopted a strategy of armor and formed exoskeleton during the ―Cambrian explosion‖ due to the 104 Unauthenticated Download Date | 1/30/17 12:55 PM Contemp.Trends.Geosci., 5(2),2016,104-112 DOI:10.1515/ctg-2016-0008 2011) It divides into three main layers The most outer layer, called periostracum, is made mostly of complex protein conchiolin Next layer – middle (mesostracum) is primarily composed of calcium carbonate crystals Third, the inner layer (hypostracum) is built by Carich carbonate plates The first two layers are formed by the edge of the mantle, and the last one by the entire surface of epithelial tissue (Urbański 1989; Dyduch-Falinowski and Piechocki 1993; Jura 2005; de Paula and Silveira 2009; Piechocki 2009) Morphology, structure and other adaptations of bivalve molluscs have critical impact on ability to survive in constantly changing environment and also to increase the probability of surviving predator attack (Vermeij 1977, 1987) The main aim of this paper is to describe the morphological diversity of microstructures present in the studied shells of some selected recent bivalve species Additionally, the authors attempt answer what is the main function of each identified structures in contexts of anti-predator adaptations Materials and methods The following species of bivalve: 1) duck mussel (Anodonta anatina Linnaeus, 1758), 2) common cockle (Cerastoderma edule Linnaeus, 1758), 3) lyrate Asiatic hard clam (Meretrix lyrata Sowerby II, 1851) and 4) blue mussel (Mytilus edulis Linnaeus, 1758), were collected from different locations All the studied shells were washed and measured (Table 1; Fig 1) Afterwards, every shell sample (one whole shell for each investigated species) was fractured in order to show the microstructural details Fractures were made parallel and perpendicular to the umbo-ventral margin axis in the central part of the valves Both left and the right valves were investigated Scanning electron microscope observation, including BSE images and EDS analyses were obtained by using a Philips XL30 ESEM/TMP equipped with EDS (EDAX type Sapphire) detector at the Faculty of Earth Sciences, University of Silesia Tab.1 Selected macroscopic characteristics of the investigated bivalve including provenance area Shell length measured from Shell height measured from Sample Bivalve species umbo to ventral margin anterior (foot) end to posterior collecting place [mm] (siphon) end [mm] Duck mussel Vistula river (Anodonta anatina) estuary Common cockle (Cerastoderma edule) Baltic Sea Lyrate Asiatic hard clam South West (Meretrix lyrata) Pacific Ocean Blue mussel (Mytilus edulis) Irish Sea 79 105 49 48 38 43 52 34 105 Unauthenticated Download Date | 1/30/17 12:55 PM Contemp.Trends.Geosci., 5(2),2016,104-112 DOI:10.1515/ctg-2016-0008 Fig.1 General morphology of studied bivalves: A) lyrate Asiatic hard clam (Meretrix lyrata), B) common cockle (Cerastoderma edule), C) duck mussel (Anodonta anatina) and D) blue mussel (Mytilus edulis) Scale bar equal to 10 cm Results Duck mussel (Anodonta anatina) Microstructures The first layer – periostracum was especially well visible in A anatina It is part, conchioline is also forming the organic matrix of the shell within which calcium carbonate is deposited (Fig 2a) Under the first layer, another duplex structure was found One part is represented by long carbonate crystal, which forms prisms The crystals are 0.1 to 0.8 mm long and 50-60 µm wide (Fig 2) Investigated prism from A anatina shell have a polygonal joint pattern both in the contact zone with periostracum and the most internal layer socalled nacreous layer, columnar nacre type (Fig 2b - lower part) The last part is built by numerous (≤1 µm) thin carbonate plates Each of the examined bivalve species is characterized by the presence of different types of microstructures They were visible in the second (mesostracum) and third (hypostracum) layer In all studied cases, the shell structures are homogenous in chemical composition, but exhibit various structures Only in one case (freshwater A anatina), the well visible presence of organic matrix is expressed by biopolymer content in obtained BSE images All structures were identified according to Grégoire (1972) and also to Carter et al (2013) 106 Unauthenticated Download Date | 1/30/17 12:55 PM Contemp.Trends.Geosci., 5(2),2016,104-112 DOI:10.1515/ctg-2016-0008 Fig.2 BSE images of microstructures in A anatina (A-B) A anatina is characterized by two, well visible layers Outer part of the shell is cover by periostracum layer, under it the bases of prismatic structure crystals are present (A) Side view of prismatic structure and Ca-rich carbonaceous plates of ―columnar nacre‖ hypostracum are also visible (B) Common cockle (Cerastoderma edule) C edule has a shell composed of a homogeneous outer layer (Fig 3a), while the lower layer is formed by fiber-like carbonate crystals (Fig 3b) This part show massive fabric comprising closely packed fiber-like calcium carbonate crystals less than µm in size, without any pores visible both macroscopically and microscopically tens of micrometers (Fig 5a) Sporadically, small pores with c.a 1-2 µm in diameter are noted Below the first layer a prismatic structure is presented (Fig 5b) It is composed of well elongated carbonate crystals They are >200 µm long and show sharp fiber-like forms with the aspect ratios